EVOLUTIONARY ADAPTATION TO ENVIRONMENTAL pH IN EXPERIMENTAL LINEAGES OF ESCHERICHIA COLI
Abstract
This study uses the enteric bacterium Escherichia coli as an experimental system to examine evolutionary responses of bacteria to an environmental acidic-alkaline range between pH 5.3 and 7.8 (15-5000 nM [H(+)]). Our goal was both to test general hypotheses about adaptation to abiotic variables and to provide insights into how coliform organisms might respond to changing conditions inside and outside of hosts. Six replicate lines of E. coli evolved for 2000 generations at one of four different constant pH conditions: pH 5.3, 6.3, 7.0, or 7.8. Direct adaptation to the evolutionary environment, as well as correlated changes in other environments, was measured as a change in fitness relative to the ancestor in direct competition experiments. The pH 5.3 group had the highest fitness gains, with a highly significant increase of 20%. The pH 7.8 group had far less significant gains and much higher variance among its lines. Analysis of individual lines within these two groups revealed complex patterns of adaptation: all of the pH 5.3 lines exhibited trade-offs (reduced fitness in another environment), but only 33% of the pH 7.8 lines showed such trade-offs and one of the pH 7.8 lines demonstrated exaptation by improving fitness in the pH 5.3 environment. Although there was also prevalent exaptation in other groups to the acidic environment, there were no such cases of exaptation to alkalinity. Comparison across the entire experimental pH range revealed that the most acidic lines, the pH 5.3 group, were all specialists, in contrast to the pH 6.3 lines, which were almost all generalists. That is, although none of the pH 5.3 lines showed any correlated fitness gains, all of the pH 6.3 lines did.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In serial batch cultures for ALE, transfer often occurs before the stationary phase is reached, which is a prerequisite to avoid stationary phase adaptation.
“As indicated in Figure 1a, in serial batch cultures for ALE, the transfer often occurs before the stationary phase is reached. Clearly, this is a prerequisite to avoid stationary phase adaptation [52].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [52]
GASP (growth advantage in stationary phase) mutants are rapidly fixed in E. coli populations.
“So-called GASP (growth advantage in stationary phase) mutants are rapidly fixed in E. coli populations [52].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [52]
Cites
Introduction to Quantitative Genetics.
Edwards, A. W. F., & Falconer, D. S. (1982) · Biometrics · doi:10.2307/2529912 · Cited by 21,447 · see citing works
Lenski, R. E., Rose, M. R., Simpson, S. C., & Tadler, S. C. (1991) · The American Naturalist · doi:10.1086/285289 · Cited by 1,582 · see citing works
Evolution Experiments with Microorganisms: The Dynamics and Genetic Bases of Adaptation
Elena, S. F., & Lenski, R. E. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1088 · Cited by 1,386 · see citing works
Measurement of gastrointestinal pH profiles in normal ambulant human subjects
Evans, D. F., Pye, G., Bramley, R., Clark, A. G., Dyson, T. J., & Hardcastle, J. D. (1988) · Gut · doi:10.1136/gut.29.8.1035 · Cited by 1,240 · see citing works
Escherichia coli acid resistance: tales of an amateur acidophile
Foster, J. W. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro1021 · Cited by 971 · see citing works
Alkaline pH homeostasis in bacteria: New insights
Padan, E., Bibi, E., Ito, M., & KRULWICH, T. A. (2005) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2005.09.010 · Cited by 808 · see citing works
Control of Acid Resistance in Escherichia coli
Castanié‐Cornet, M., Penfound, T. A., Smith, D. K., et al. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.11.3525-3535.1999 · Cited by 626 · see citing works
Mechanisms of acid resistance in enterohemorrhagic Escherichia coli
Lin, J.-S., Smith, M. P., Chapin, K. C., Baik, H. S., Bennett, G. N., & Foster, J. W. (1996) · Applied and Environmental Microbiology · doi:10.1128/aem.62.9.3094-3100.1996 · Cited by 574 · see citing works
Lin, J.-S., Lee, I. S., Frey, J., Slonczewski, J. L., & Foster, J. W. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.14.4097-4104.1995 · Cited by 569 · see citing works
An Introduction to Quantitative Genetics
Crusio, W. E. (2006) · CRC Press eBooks · doi:10.1201/9781420003567.ch4 · Cited by 493 · see citing works
Fitness of RNA virus decreased by Muller’s ratchet
Chao, L. (1990) · Nature · doi:10.1038/348454a0 · Cited by 488 · see citing works
Acid resistance in enteric bacteria
Gorden, J., & Small, P. L. C. (1993) · Infection and Immunity · doi:10.1128/iai.61.1.364-367.1993 · Cited by 454 · see citing works
Acid and base resistance in Escherichia coli and Shigella flexneri: role of rpoS and growth pH
Small, P. L. C., Blankenhorn, D., Welty, D. M., et al. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.6.1729-1737.1994 · Cited by 432 · see citing works
Trade‐Offs in Thermal Adaptation: The Need for a Molecular to Ecological Integration
Pörtner, H., Bennett, A. F., Bozinovic, F., Clarke, A., Lardies, M. A., Lucassen, M., Pelster, B., Schiemer, F., & Stillman, J. H. (2006) · Physiological and Biochemical Zoology · doi:10.1086/499986 · Cited by 414 · see citing works
Self-citationRichard, H., & Foster, J. W. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.18.6032-6041.2004 · Cited by 388 · see citing works
Protons, osmolytes, and fitness of internal milieu for protein function
Somero, G. N. (1986) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1986.251.2.r197 · Cited by 340 · see citing works
Biase, D. D., Tramonti, A., Bossa, F., & Visca, P. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01430.x · Cited by 280 · see citing works
Breaking through the acid barrier: An orchestrated response to proton stress by enteric bacteria
Audia, J. P., Webb, C. C., & Foster, J. W. (2001) · International Journal of Medical Microbiology · doi:10.1078/1438-4221-00106 · Cited by 258 · see citing works
Lenski, R. E. (1988) · Evolution · doi:10.1111/j.1558-5646.1988.tb04149.x · Cited by 258 · see citing works
Bennett, A. F., Lenski, R. E., & Mittler, J. E. (1992) · Evolution · doi:10.1111/j.1558-5646.1992.tb01981.x · Cited by 252 · see citing works
Self-citationA glutamate-dependent acid resistance gene in Escherichia coli
Hersh, B. M., Farooq, F. T., Barstad, D. N., et al. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.13.3978-3981.1996 · Cited by 245 · see citing works
K+, Na+, and Cl- activities in ventricular myocytes isolated from rabbit heart
Désilets, M., & Baumgarten, C. M. (1986) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1986.251.2.c197 · Cited by 233 · see citing works
Escherichia coli intracellular pH, membrane potential, and cell growth
Zilberstein, D., AGMON, V., Schuldiner, S., & Padan, E. (1984) · Journal of Bacteriology · doi:10.1128/jb.158.1.246-252.1984 · Cited by 222 · see citing works
EVOLUTIONARY ADAPTATION TO TEMPERATURE II. THERMAL NICHES OF EXPERIMENTAL LINES OF ESCHERICHIA COLI
Bennett, A. F., & Lenski, R. E. (1993) · Evolution · doi:10.1111/j.1558-5646.1993.tb01194.x · Cited by 204 · see citing works
Self-citationRelative fitness can decrease in evolving asexual populations of S. cerevisiae
Paquin, C. E., & Adams, J. (1983) · Nature · doi:10.1038/306368a0 · Cited by 188 · see citing works
Rapid evolution in response to high-temperature selection
Bennett, A. F., Dao, K. M., & Lenski, R. E. (1990) · Nature · doi:10.1038/346079a0 · Cited by 182 · see citing works
Self-citationTHERMAL SENSITIVITY OF DROSOPHILA MELANOGASTER RESPONDS RAPIDLY TO LABORATORY NATURAL SELECTION
Huey, R. B., Partridge, L., & Fowler, K. (1991) · Evolution · doi:10.1111/j.1558-5646.1991.tb04343.x · Cited by 181 · see citing works
Lenski, R. E. (1988) · Evolution · doi:10.1111/j.1558-5646.1988.tb04150.x · Cited by 168 · see citing works
Lenski, R. E. (1988) · Evolution · doi:10.2307/2409028 · Cited by 153 · see citing works
Hickey, E. W., & Hirshfield, I. N. (1990) · Applied and Environmental Microbiology · doi:10.1128/aem.56.4.1038-1045.1990 · Cited by 125 · see citing works
Escherichia coli acid resistance: pH‐sensing, activation by chloride and autoinhibition in GadB
Gut, H., Pennacchietti, E., John, R., Bossa, F., Capitani, G., Biase, D. D., & Grütter, M. (2006) · EMBO Journal · doi:10.1038/sj.emboj.7601107 · Cited by 101 · see citing works
Bennett, A. F., Lenski, R. E., & Mittler, J. E. (1992) · Evolution · doi:10.2307/2409801 · Cited by 90 · see citing works
Self-citationEVOLUTIONARY ADAPTATION TO TEMPERATURE. IV. ADAPTATION OF ESCHERICHIA COLI AT A NICHE BOUNDARY
Mongold, J. A., Bennett, A. F., & Lenski, R. E. (1996) · Evolution · doi:10.1111/j.1558-5646.1996.tb04470.x · Cited by 85 · see citing works
Self-citationThermal Sensitivity of Drosophila melanogaster Responds Rapidly to Laboratory Natural Selection
Huey, R. B., Patridge, L., & Fowler, K. (1991) · Evolution · doi:10.2307/2409925 · Cited by 84 · see citing works
Evolutionary Adaptation to Temperature II. Thermal Niches of Experimental Lines of Escherichia coli
Bennett, A. F., & Lenski, R. E. (1993) · Evolution · doi:10.2307/2410113 · Cited by 77 · see citing works
Self-citationLenski, R. E. (1988) · Evolution · doi:10.2307/2409029 · Cited by 73 · see citing works
An Experimental Evolutionary Study on Adaptation to Temporally Fluctuating pH inEscherichia coli
Hughes, B. S., Cullum, A. J., & Bennett, A. F. (2007) · Physiological and Biochemical Zoology · doi:10.1086/518353 · Cited by 54 · see citing works
Self-citationBennett, A. F., & Lenski, R. E. (1996) · Evolution · doi:10.1111/j.1558-5646.1996.tb03862.x · Cited by 38 · see citing works
Self-citationEvolutionary Adaptation to Temperature. IV. Adaptation of Escherichia coli at a Niche Boundary
Mongold, J. A., Bennett, A. F., & Lenski, R. E. (1996) · Evolution · doi:10.2307/2410778 · Cited by 31 · see citing works
Self-citationHicks, W. M., Kotlajich, M. V., & Visick, J. E. (2005) · Microbiology · doi:10.1099/mic.0.27835-0 · Cited by 26 · see citing works
Stewart, N. T., Feng, J., Liu, X., et al. (2005) · Microbiology · doi:10.1099/mic.0.28022-0 · Cited by 16 · see citing works
Bennett, A. F., & Lenski, R. E. (1996) · Evolution · doi:10.2307/2410825 · Cited by 11 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Adaptive laboratory evolution—Principles and applications for biotechnology
Dragosits, M., & Mattanovich, D. (2013) · Microbial Cell Factories · doi:10.1186/1475-2859-12-64 · Cited by 827 · see citing works
Dhar, R., Sägesser, R., Weikert, C., & Wagner, A. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mss253 · Cited by 126 · see citing works
Microbial experimental evolution
Bennett, A. F., & Hughes, B. S. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90562.2008 · Cited by 58 · see citing works
Self-citationMicrobial evolution in vivo and in silico: methods and applications
Mozhayskiy, V., & Tagkopoulos, I. (2013) · Integr. Biol. · doi:10.1039/c2ib20095c · Cited by 24 · see citing works
- Authors
- Hughes, B. S., Cullum, A. J., & Bennett, A. F.
- Affiliations
- University of California, Irvine (US)
- Creighton University (US)
- Corresponding author
- Hughes, Bradley S.
- ORCID
- Cullum, Alistair J.
- Venue
- Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2007-07
- Volume
- 61
- Issue
- 7
- Pages
- 1725-1734
- ISSN
- 0014-3820 (ISSN-L)
- 1558-5646
- OpenAlex
- W2136965666
- Cited by
- 71
- References
- 42
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 4 · 2023: 1 · 2022: 1 · 2021: 3 · 2020: 11 · 2019: 4 · 2018: 6 · 2017: 2 · 2016: 5 · 2015: 3 · 2014: 4 · 2013: 7 · 2012: 6
- FWCI
- 1.08
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Evolution (publishedVersion)
- PubMed (publishedVersion)
- BioOne Complete (BioOne) (submittedVersion)
- Funders
- National Science Foundation
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Social Sciences › Cultural Studies › Language and cultural evolution
- Social Sciences › Arts and Humanities › History and Philosophy of Science › Philosophy and History of Science
- Keywords
- Escherichia coli, pH adaptation, acid resistance, alkaline tolerance, experimental evolution, fitness trade-offs, exaptation, coliform bacteria
- MeSH terms
- Adaptation, Physiological, Escherichia coli, Biological Evolution, Hydrogen-Ion Concentration
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review